Abstract
The asymmetric localization of proteins in the plasma membrane domains of eukaryotic cells is a fundamental manifestation of cell polarity that is central to multicellular organization and developmental patterning. In plants, the mechanisms underlying the polar localization of cargo proteins are still largely unknown and appear to be fundamentally distinct from those operating in mammals. Here, we present a systematic, quantitative comparative analysis of the polar delivery and subcellular localization of proteins that characterize distinct polar plasma membrane domains in plant cells. The combination of microscopic analyses and computational modeling revealed a mechanistic framework common to diverse polar cargos and underlying the establishment and maintenance of apical, basal, and lateral polar domains in plant cells. This mechanism depends on the polar secretion, constitutive endocytic recycling, and restricted lateral diffusion of cargos within the plasma membrane. Moreover, our observations suggest that polar cargo distribution involves the individual protein potential to form clusters within the plasma membrane and interact with the extracellular matrix. Our observations provide insights into the shared cellular mechanisms of polar cargo delivery and polarity maintenance in plant cells.
Highlights
The asymmetric distribution of proteins is a prerequisite of many cellular processes such as cell division, intracellular communication, nutrient transport, tissue morphogenesis, and cell differentiation [1,2,3]
To characterize systematically the different polar PM domains in plant cells, we evaluated quantitatively the subcellular localization of the green fluorescent protein (GFP)-fused polar cargos PIN1-GFP [42], PIN2-GFP [43], GFP-ABCG37 [44], ABCG36-GFP [45], and BOR1-GFP [40], and compared with the non-polar plasma membrane intrinsic protein 2A (PIP2-GFP; [46]) marker in roots of Arabidopsis thaliana
To test whether super-polar recycling to a particular polar domain is typically associated with polar cargos or applies to all PM proteins, we examined recycling of non-polar PIP2-GFP to outer and transversal cell sides
Summary
The asymmetric distribution of proteins is a prerequisite of many cellular processes such as cell division, intracellular communication, nutrient transport, tissue morphogenesis, and cell differentiation [1,2,3]. Endodermis cells can become encircled by lignin bands [6] called Casparian strips, which act as physical barriers on the radial and transverse walls to restrict the exchange of water and nutrients [7]. This polar band can separate outer and inner polar domains in endodermal cells, it does not interfere with the apical and basal polarization [8]. These findings suggest that plants have acquired a unique strategy to generate and maintain the subcellular polar distribution of proteins in the PM [9,10,11]
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